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Title: Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape

Abstract

Single genome sequencing of early HIV-1 genomes provides a sensitive, dynamic assessment of virus evolution and insight into the earliest anti-viral immune responses in vivo. By using this approach, together with deep sequencing, site-directed mutagenesis, antibody adsorptions and virus-entry assays, we found evidence in three subjects of neutralizing antibody (Nab) responses as early as 2 weeks post-seroconversion, with Nab titers as low as 1:20 to 1:50 (IC50) selecting for virus escape. In each of the subjects, Nabs targeted different regions of the HIV-1 envelope (Env) in a strain-specific, conformationally sensitive manner. In subject CH40, virus escape was first mediated by mutations in the V1 region of the Env, followed by V3. HIV-1 specific monoclonal antibodies from this subject mapped to an immunodominant region at the base of V3 and exhibited neutralizing patterns indistinguishable from polyclonal antibody responses, indicating V1–V3 interactions within the Env trimer. In subject CH77, escape mutations mapped to the V2 region of Env, several of which selected for alterations of glycosylation. And in subject CH58, escape mutations mapped to the Env outer domain. In all three subjects, initial Nab recognition was followed by sequential rounds of virus escape and Nab elicitation, with Nab escape variants exhibiting variablemore » costs to replication fitness. Although delayed in comparison with autologous CD8 T-cell responses, our findings show that Nabs appear earlier in HIV-1 infection than previously recognized, target diverse sites on HIV-1 Env, and impede virus replication at surprisingly low titers. The unexpected in vivo sensitivity of early transmitted/ founder virus to Nabs raises the possibility that similarly low concentrations of vaccine-induced Nabs could impair virus acquisition in natural HIV-1 transmission, where the risk of infection is low and the number of viruses responsible for transmission and productive clinical infection is typically one.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [2];  [2];  [2];  [2];  [2];  [5];  [5];  [1];  [1];  [3];  [6];  [7];  [5];  [5];  [4] more »;  [4];  [2];  [2];  [2];  [1];  [4];  [1] « less
+ Show Author Affiliations
  1. Univ. of Pennsylvania, Philadelphia, PA (United States). Perelman School of Medicine
  2. Duke Univ., Durham, NC (United States). School of Medicine
  3. Univ. of Alabama, Birmingham, AL (United States)
  4. National Institutes of Health (NIH), Bethesda, MD (United States). National Inst. of Allergy and Infectious Disease. Vaccine Research Center
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  6. National Cancer Institute, Frederick, MD (United States). SAIC-Frederick Inc.
  7. Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1627903
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 8; Journal Issue: 5; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; Parasitology; Virology

Citation Formats

Bar, Katharine J., Tsao, Chun-yen, Iyer, Shilpa S., Decker, Julie M., Yang, Yongping, Bonsignori, Mattia, Chen, Xi, Hwang, Kwan-Ki, Montefiori, David C., Liao, Hua-Xin, Hraber, Peter, Fischer, William, Li, Hui, Wang, Shuyi, Sterrett, Sarah, Keele, Brandon F., Ganusov, Vitaly V., Perelson, Alan S., Korber, Bette T., Georgiev, Ivelin, McLellan, Jason S., Pavlicek, Jeffrey W., Gao, Feng, Haynes, Barton F., Hahn, Beatrice H., Kwong, Peter D., and Shaw, George M. Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape. United States: N. p., 2012. Web. doi:10.1371/journal.ppat.1002721.
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Bar, Katharine J., Tsao, Chun-yen, Iyer, Shilpa S., Decker, Julie M., Yang, Yongping, Bonsignori, Mattia, Chen, Xi, Hwang, Kwan-Ki, Montefiori, David C., Liao, Hua-Xin, Hraber, Peter, Fischer, William, Li, Hui, Wang, Shuyi, Sterrett, Sarah, Keele, Brandon F., Ganusov, Vitaly V., Perelson, Alan S., Korber, Bette T., Georgiev, Ivelin, McLellan, Jason S., Pavlicek, Jeffrey W., Gao, Feng, Haynes, Barton F., Hahn, Beatrice H., Kwong, Peter D., & Shaw, George M. Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape. United States. https://doi.org/10.1371/journal.ppat.1002721
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Bar, Katharine J., Tsao, Chun-yen, Iyer, Shilpa S., Decker, Julie M., Yang, Yongping, Bonsignori, Mattia, Chen, Xi, Hwang, Kwan-Ki, Montefiori, David C., Liao, Hua-Xin, Hraber, Peter, Fischer, William, Li, Hui, Wang, Shuyi, Sterrett, Sarah, Keele, Brandon F., Ganusov, Vitaly V., Perelson, Alan S., Korber, Bette T., Georgiev, Ivelin, McLellan, Jason S., Pavlicek, Jeffrey W., Gao, Feng, Haynes, Barton F., Hahn, Beatrice H., Kwong, Peter D., and Shaw, George M. Thu . "Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape". United States. https://doi.org/10.1371/journal.ppat.1002721. https://www.osti.gov/servlets/purl/1627903.
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@article{osti_1627903,
title = {Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape},
author = {Bar, Katharine J. and Tsao, Chun-yen and Iyer, Shilpa S. and Decker, Julie M. and Yang, Yongping and Bonsignori, Mattia and Chen, Xi and Hwang, Kwan-Ki and Montefiori, David C. and Liao, Hua-Xin and Hraber, Peter and Fischer, William and Li, Hui and Wang, Shuyi and Sterrett, Sarah and Keele, Brandon F. and Ganusov, Vitaly V. and Perelson, Alan S. and Korber, Bette T. and Georgiev, Ivelin and McLellan, Jason S. and Pavlicek, Jeffrey W. and Gao, Feng and Haynes, Barton F. and Hahn, Beatrice H. and Kwong, Peter D. and Shaw, George M.},
abstractNote = {Single genome sequencing of early HIV-1 genomes provides a sensitive, dynamic assessment of virus evolution and insight into the earliest anti-viral immune responses in vivo. By using this approach, together with deep sequencing, site-directed mutagenesis, antibody adsorptions and virus-entry assays, we found evidence in three subjects of neutralizing antibody (Nab) responses as early as 2 weeks post-seroconversion, with Nab titers as low as 1:20 to 1:50 (IC50) selecting for virus escape. In each of the subjects, Nabs targeted different regions of the HIV-1 envelope (Env) in a strain-specific, conformationally sensitive manner. In subject CH40, virus escape was first mediated by mutations in the V1 region of the Env, followed by V3. HIV-1 specific monoclonal antibodies from this subject mapped to an immunodominant region at the base of V3 and exhibited neutralizing patterns indistinguishable from polyclonal antibody responses, indicating V1–V3 interactions within the Env trimer. In subject CH77, escape mutations mapped to the V2 region of Env, several of which selected for alterations of glycosylation. And in subject CH58, escape mutations mapped to the Env outer domain. In all three subjects, initial Nab recognition was followed by sequential rounds of virus escape and Nab elicitation, with Nab escape variants exhibiting variable costs to replication fitness. Although delayed in comparison with autologous CD8 T-cell responses, our findings show that Nabs appear earlier in HIV-1 infection than previously recognized, target diverse sites on HIV-1 Env, and impede virus replication at surprisingly low titers. The unexpected in vivo sensitivity of early transmitted/ founder virus to Nabs raises the possibility that similarly low concentrations of vaccine-induced Nabs could impair virus acquisition in natural HIV-1 transmission, where the risk of infection is low and the number of viruses responsible for transmission and productive clinical infection is typically one.},
doi = {10.1371/journal.ppat.1002721},
journal = {PLoS Pathogens},
number = 5,
volume = 8,
place = {United States},
year = {Thu May 31 00:00:00 EDT 2012},
month = {Thu May 31 00:00:00 EDT 2012}
}
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https://doi.org/10.1371/journal.ppat.1002721
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